Evolution of a sex ratio observed


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If you’ve been reading that fascinating graphic novel, Y: The Last Man(amzn/b&n/abe/pwll), you know the premise: a mysterious disease has swept over the planet and bloodily killed every male mammal except two, a human named Yorick and a monkey named Ampersand. Substantial parts of it are biologically nearly impossible: the wide cross-species susceptibility, the near instantaneous lethality, and the simultaneity of its effect everywhere (there are also all kinds of weird correlations with other sort of magical putative causes, which may be red herrings). On the other hand, the sociological part of the story seems very plausible. There is no feminist utopia, the world goes on in a traumatized and rather complicated way, and the reactions everywhere vary from crazed euphoria to a more common despair. One thing that isn’t at all implausible, and actually has been observed, is a plague that selectively exterminates males.

It’s called Wolbachia. It’s not quite as dramatic as the plague that turns males into hemorrhaging corpses in the graphic novel — it kills developing males as embryos, or more sneakily, disrupts sex determination so that all the embryos develop as females. This is advantageous to the bacterium, because it is transmitted in the cytoplasm of the egg, so males won’t pass it on to their progeny and are useless from the point of view of Wolbachia. It is, like the plague in Y, something that infects a huge range of species, but each species varies in the severity of its response to the bacterium.

My readers with simple camera eyes will be relieved to know that the disease only affects arthropods. Those of you with compound eyes ought to worry: Wolbachia is also being being considered for use as a biological pesticide.

Now here’s a disease that can have dramatic effects on a population—in some cases, the sex ratio can shift from 50:50 females:males to 99:1. That can be devastating to a population, although of course it’s nowhere near as severe as if that ratio were reversed. Here’s where evolution comes into play. What if a mutation for resistance to the sex-distorter effects of Wolbachia arose? What if, say, one of the rare males carried an allele that made his male progeny able to fight off the deleterious effects of infection with Wolbachia?

I think you can guess. That would be a greatly beneficial mutation that would spread with extraordinary rapidity. Since the rare male carriers would face little competition and would be fertilizing many females, they ought to produce lots of progeny and lots more males, who would spread the resistance further.

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Now such an example of evolution in action has been directly observed. Butterflies of the species Hypolimnas bolina, the Blue Moon butterfly, in the Polynesian islands have been known for several years to be suffering from an extreme case of the sex-ratio distorter infection, with populations consisting of greater than 99% females. In 2005-2006, males were found to be making a comeback, and a complete shift from a highly skewed sex ratio to the more normal 50:50 proportions was observed to occur in only 10 generations — about a year. It’s a beautiful example of how rapidly natural selection can transform a population when selection pressures are high.

The cause of the change is not eradication of Wolbachia — the animals are still carrying the bacterium. It is also not a result of the bacterium reducing its virulence autonomously, since introgression of Wolbachia from resistant populations into susceptible ones showed a full return of the male-killing ability of the bacterium. Something in the nuclear genome of the butterfly had changed to confer resistance.

Now here’s one thing that bugs me about Y: The Last Man. For this rapid dispersal of resistance to spread, resistant males should be procreating profligately. In the book, Yorick seems to be obstinately abstinent! (Some of the women, at least, understand the principle, and there are plots with attempts to capture the last man for breeding stock for their group.) I can understand how the author might want to resist turning the story into a boring male fantasy of having the only penis among teeming millions of fertile females, but come on, biological reality has to intrude at some point. The future of the human race demands it!


Charlat S, Hornett EA, Fullard JH, Davies N, Roderick GK, Wedell N, Hurst GDD (2007) Extraordinary flux in sex ratio. Science 317:214.

Comments

  1. J Daley says

    Jebus, this is a good article. Fascinating, entertaining – you just get better and better.

  2. says

    Just an interesting aside: Frank Herbert (he of Dune fame) wrote a novel in the ’80s (The White Plague) that centered around a biologist who, overcome by grief at the death of his wife and children at the hands of terrorists, genetically engineers a virus that targets women and nearly wipes out the female population of the world. An interesting read…

  3. Rey Fox says

    On the topic of Y: The Last Man, no spoilers, please! I’ve been reading through the series at the local library, and have only got to their arrival in Japan.

  4. Will says

    There is a great short story by James Tiptree (nee Alice Sheldon – one of the greatest writers of science fiction)
    called “Houston, Houston, Do You Read?” that covers this very idea. The women clone themselves so they can go on as a society (a much smaller society) without men. When they do find some men (astronauts shot forward in time in a bizarre accident), they decide they don’t need them since the only purpose of men is to protect women and children from other men… In that story though, I believe that the defect that wiped out the men was on the X chromosome and caused only girls to be born, or something like that.

  5. Firemancarl says

    Well, thanks PZ! That was MY fantasy! The only living male, I would have multiple subject to do my bidding bwahahahahahaha.

    Que cheesy sax music.

  6. Diatryma says

    Sheldon/Tiptree had another one, “The Screwfly Solution”, with something like this happening. And Joanna Russ’ “When It Changed” has a social perspective of it. Quite a few writers have batted the idea around, but those are the two I always remember.

  7. says

    In the book, Yorick seems to be obstinately abstinent! (Some of the women, at least, understand the principle, and there are plots with attempts to capture the last man for breeding stock for their group.)

    Well, reproductive biology shows us that there is a compromise position, as well–with electroejaculation, everybody wins.

  8. Dianne says

    Those of you with compound eyes ought to worry

    I initially read this as “Those of US with compound eyes…” and was briefly concerned that either there was something PZ wasn’t telling us about himself or he had had a recent accident with a teleporter…

  9. tceisele says

    Yes, the whole setup in “Y: The Last Man” bugs me no end. First off, the government should be vigorously guarding every sperm bank in the country, and impregnating as many women as possible. Even if all the “Y” sperm are dead, raising up a new generation of girls will buy time. Meanwhile, Our Protagonist shouldn’t be letting anything go to waste. Heck, it might be better if he *didn’t* actually have sex with women. With proper managment, subdivision into the minimum effective dosages, artificial insemination, and selection of women at the optimum time, they should be getting multiple pregnancies for every ejaculation. Heck, with highly-developed in-vitro fertilization (or maybe just some advanced work with an endoscope), they might be able to manage something approaching 1 sperm = 1 pregnancy if they really tried hard. And the sooner he starts, the sooner there are likely to be sons to take some of the load off of the soon-to-be-father-of-his-country. But nooooooo, he’s sloughing off his responsibilities and not even leaving a trail of children in his wake . . .

  10. Caledonian says

    One sperm, one pregnancy would probably be a very poor way of arranging things, given that sperm tend to be manufactured suboptimally and many of which are defective.

    The long journey through the female reproductive tract is partially a method for screening out those spermatozoa that are inefficient and thus more likely to carry DNA defects.

    If you went out of your way to select the best sperm out of ten thousand, you could still have hundreds of pregnancies from each ejacuation.

  11. aweb says

    To those poking holes in the Y Last Man storyline : read the books, the author has dealt with many of them. The implausibility of the whole setup was acknowledged with a wink and a nod to the audience in the latest issue. Sperm banks were targeted for destruction by “amazon” gangs. Yorick does have at least one child (not a minor plot point). The US government understandably becomes mostly irrelevant after half the population dies a horrible death all at once, taking with it most of the armed forces, army, elected representatives, police, firefighters, majority of doctors, etc etc…Also, it’s a fantasy comic book concept to tell interesting stories around. Filling in every possible plot hole would take too long.

  12. CaseyL says

    Pity Wolbachia can’t be tailored specifically for humans. It’d be a great non-violent, non-lethal way to quickly and drastically reduce the human population back to something the ecosphere might actually survive.

  13. _Arthur says

    Robert Merle, a , wrote “The Virility Factor”, 1977, where the US and the world is devastated by a plague that strike men and men alone.

    In the resulting society, men have a much reduced social status, and are gigolos or trophy spouses.

  14. Kagehi says

    Was an episode of one of those more recent Twilight Zone clone shows that had this idea too. Some group of women who had power and access to labs invent a virus that specifically targets men, on the grounds that men are the cause of all the problems in the world. They also manage to develop cloning or something to the point where they can maintain the female population after its released. Some where along the line one group gets some DNA out of a grave some place, then tries to *engineer* a male without all those nasty aggressive tendencies, the powers that be eventually find out, and lo and behold, he shoots one of them anyway, while defending the life of one of the women trying to protect him. After, everything goes on as before, except there is some small group of women that now know the truth about what happened and are more likely to defend the next one that comes along, or maybe even the child one of them is carrying, if that happened to be male.

    That is, if I am remembering the story right. Its a fairly common theme it seems.

  15. says

    I’ll have to check out Y: The Last Man.

    Maybe he’s gay. MWUAHAHAHA! now THAT would be fun. Have the women of earth try to catch him, while he runs away, horrified.

    What a tragedy.

  16. clem says

    The butterfly incident is fascinating. Have they detected any deleterious effects from the male population being dragged through a genetic knothole?

  17. says

    “Wolbachia is also being being considered for use as a biological pesticide.”

    Personally, I’m kind of freaking out about this. A mutated version gets into the bee population, it’s not just bad news for the compound eye brigade. Those of us who live largely on pollinated plants, or on animals who live largely on pollinated plants, are potentially in big trouble.

    I’m just sayin’, is all.

  18. Rey Fox says

    “It’d be a great non-violent, non-lethal way to quickly and drastically reduce the human population back to something the ecosphere might actually survive.”

    As long as you don’t mind certain cultures descending into chaos in the meantime. Probably not as nonlethal as all that.

  19. Chris says

    #19: They murder three billion people and then try to eliminate aggressive tendencies from the *other* sex?

    Sadly, I can actually imagine human beings thinking like that. But it’s pretty staggering when you think about it.

  20. Vasha says

    Yet another such science fiction work: “In the Mothers’ Land” by Elisabeth Vonarburg, which I reviewed here. Like most, if not all, such sf, the author is shaky on the biology of how the human population comes to have a nearly 100-to-1 female-to-male ratio, and concentrates on the social aspects (well developed).

  21. says

    And on the other side of the coin, Cordwainer Smith’s story “The Crime and Glory of Commander Suzdal” posits the existence of a world where the women “succumb[ed] to a plague that (in Smith’s words) rendered ‘femininity carcinogenic.'”

    It’s not any prettier than the all-women worlds.

  22. False Prophet says

    A somewhat similar tale, though with religious overtones, was a DC graphic novel from the early 90s, Me and Joe Priest.

    Basically, all men and most women become sterile (referred to as the “drying up”) and civilization is slowly grinding down–not as violently as the film Children of Men but still in descent. Only a single Catholic priest remains fertile, and he believes he is sent by God to repopulate the Earth. Accompanied by his bodyguard, a Special Forces soldier cum biker nomad, Father Joseph goes around inseminating the remaining fertile young women (guided by a star in the sky). Meanwhile, the remnants of the Catholic Church have become a death cult (or, more of a death cult than normal) of assassins and set out to eliminate the good father, as they believe the drying up is God’s punishment upon a sinful humanity.

    Yeah, it sounds like a hokey religious tale, but the revelation at the end might win you back.

  23. Hungry Hungry Tauren says

    Vertigo has been producing some really great stuff lately, Y: The Last Man and DMZ in particular. I’m more of a Marvel guy myself (No More Mutants! Who’s Side Are You On? You’re acting kinda Skrully…) having lost all taste for mainstream DC stuff (mainly due to a lack of interest and Cassandra Cain turning evil for no fucking reason, though Sinestro Corps looks cool). Everything Brian K. Vaughn seems to touch turns out golden, from Runaways to Y to the Hood. Excellent post, PZ! Very informative, and tying this stuff into comics never hurts.

    Though you’ve been acting a bit Skrullish lately…

  24. Caledonian says

    In one of Ursula K. Le Guin’s short stories of the Ekumen, there’s a planet engineered so that only one out of every seventeen births is male. “The Matter of Seggri”. The resulting society is horrifying, as it is intended to be.

  25. Me says

    “Now here’s one thing that bugs me about Y: The Last Man. For this rapid dispersal of resistance to spread, resistant males should be procreating profligately. In the book, Yorick seems to be obstinately abstinent!”

    That’s assuming his immunity is in his genes instead of a trait he acquired later…

  26. Caledonian says

    The fact that a single human male, and a single male monkey, escaped a plague that slaughtered every other mammalian male, strongly suggests that it’s not a matter of genetics.

  27. Anonomouse says

    “Substantial parts of it are biologically nearly impossible: the wide cross-species susceptibility, the near instantaneous lethality, and the simultaneity of its effect everywhere ”

    It’s Entertainment.

    You’re supposed to use suspension of disbelief.

  28. NelC says

    One of the protagonists in Joanna Russ’ The Female Man is from a future where men have been rendered extinct so that they must reproduce through cloning. Yet another is from a future where men and women have suffered a terrible war between the sexes, and now live separate lives, hating each other; they reproduce by the men trading their sperm for various goods with the women.

  29. says

    “It’s not any prettier than the all-women worlds.”

    Actually, I thought Whileaway — the all-female world in Joanna Russ’s “When It Changed” — didn’t suck. It’s actually pretty high on my list of fictional places I might like to live, or at least visit (although Bellona from Dahlgren probably tops the list).

    And no, I don’t hate men. I quite like men. I just thought it was an interesting and non-sucky world.

  30. Torbjörn Larsson, OM says

    Yorick seems to be obstinately abstinent!

    Alas, poor Yorick! Y is such a fragile thing to be.

  31. Torbjörn Larsson, OM says

    Yorick seems to be obstinately abstinent!

    Alas, poor Yorick! Y is such a fragile thing to be.

  32. PMembrane says

    I’ve only read the amazon.com sampler, but does anyone find it rather odd that the policewoman chooses to off herself less than 25 minutes into the plague–long before anyone could possibly have a clear idea of just what was going on, and rather less time than it would normally take for some sort of existential despair to set in?

    Kagehi@19: I believe you are confusing two different stories–one was the New Outer Limits episode “Lithia”, which involved the aftermath of a full-scale nuclear and biological war that killed 99.7% of the female population and 100% of the male population.

    The other is the 1999 TV movie The Last Man on Planet Earth in which the U.S. uses a genetically-engineered “Y-Bomb” to kill the male population of Afganistan, but is caught off-guard when the pathogen mutates into a communicable form that kills 99.9% of the world’s men. In the ensuing hysteria a woman begins a movement to prohibit the birth of any male children, when she is assassinated she is hailed as a martyr and her ideology is made law. (The rest of the story is as you wrote.)

  33. says

    Nobody has mentioned Philip Wylie’s 1951 novel “The Disappearance,” wherein “an unexplained cosmic “blink” splits humanity along gender lines into two divergent timelines: from the men’s perspective, all the women disappear and from the women’s, all men vanish.” Guess which one prospers and which withers? (http://en.wikipedia.org/wiki/Philip_Wylie)

    I also would mention Lois McMaster Bujold’s 1986 Barrayar side-story, “Ethan of Athos,” a planetary society that uses uterine replicators to maintain the all-male-only population.
    (http://en.wikipedia.org/wiki/Ethan_of_Athos)

  34. PMembrane says

    Chris @ 28

    #19: They murder three billion people and then try to eliminate aggressive tendencies from the *other* sex?

    See above, they were only trying to kill 11 million people, the other 3 billion simply came as a bonus. :)

  35. PMembrane says

    The US government understandably becomes mostly irrelevant after half the population dies a horrible death all at once, taking with it most of the armed forces, army, elected representatives, police, firefighters, majority of doctors, etc etc…

    Still, I imagine that institutions would survive in some form, though large political units very likely would not withstand the ensuing upheaval. (Of course, if the upheaval is so large enough that ICBMs start flying around then all bets are off.)

  36. Skeptic8 says

    An old “report” suggests some immunity to HIV was found amongst SAfrica prostitutes. Hmm-m; does our “junk DNA” have a protected or mutated “pattern” in the in the toolbox from the last time we met this SIV pandemic?

  37. djlactin says

    A couple other sci-fi stories with the one-gender-is-vanishingly-rare theme.

    “A boy and his dog” by Harlan Ellison (also made into a movie starring a very young Don Johnson.) Post-apocalypse, most humans live below ground, but can’t seem to produce sons. Kidnap our hero and ‘use’ him as a donor (cue the electroejaculator). This is only one subplot of a (standard for Ellison) bizarre and disturbing story.

    The Tleilaxu in the DUNE series. No-one has ever seen a Tleilaxu female. But then there are the Axlotl “tanks”….

    SPOILER alert: The Honored Matres (mmmph!)

  38. Ian says

    Alas, Poor Yorick! I knew him…a ratio of 3,000,000,000 to 1!

    But we know all those butterflies were killed not by a parasite, but by being nailed to trees to fake photographs for evolution textbooks….

  39. David Marjanović says

    An old “report” suggests some immunity to HIV was found amongst SAfrica prostitutes. Hmm-m; does our “junk DNA” have a protected or mutated “pattern” in the in the toolbox from the last time we met this SIV pandemic?

    Nope. A simple mutation that has, incidentally, been found in other people as well. Has nothing to do with junk DNA.

  40. David Marjanović says

    An old “report” suggests some immunity to HIV was found amongst SAfrica prostitutes. Hmm-m; does our “junk DNA” have a protected or mutated “pattern” in the in the toolbox from the last time we met this SIV pandemic?

    Nope. A simple mutation that has, incidentally, been found in other people as well. Has nothing to do with junk DNA.

  41. PennyBright says

    Hrmph. Charlotte Perkins Gilman wrote it first. Herland, 1915. You can read it online at Project Gutenberg.

    We’ve been dreaming about a world without you males for *centuries*. ;)

  42. Rene says

    Without men, most engineers, chemists, physicists, computer scientists, surgeons, construction workers, maintenance workers, pilots, ship’s captains and crew, rail workers, architects, farmers, truckers, etc. etc. would be gone in short order.

    It would be a very primitive life with little likelihood of improving, or finding a cure.

    Hey! Would you empty that chamberpot, and patch up that thatched roof while you’re at it!

  43. Ken Mareld says

    Thank you djlactin. I too was reminded of ‘A Boy and His Dog’ by Harlan Ellison. Great story, campy movie. In the movie he ate the dog, after escaping those who wanted his sperm without the joy of sex. Not less realistic (yes, I intended that perversion of grammar) is Dr. Strangelove’s plan for repopulating the planet. Dr. Strangelove, my number two favorite movie.

    Ken

  44. says

    Y pretty much says (I refuse to consider this a spoiler) that all the males were killed by magic, which pretty much moots any complaints about implausibility. Still a good yarn.

    Also, I second the recommendation of Runaways. Of course, if we’re talking about any and all comics in general, there’s Blankets, Bone, Concrete, Ex Machina… Especially Blankets; I think some folks here would like it–it’s the author’s memoir of growing up in a devout, insular Christianity, and growing out of it as he matures.

  45. says

    I work on Wolbachia too, primarily from an ecological perspective, but I’m familiar with a broad range of the relevant literature. Wolbachia has been experimentally introduced into previously uninfected insects in the laboratory, but its effects in a new host are currently unpredictable. I write “currently” because there are lots of labs investigating its effects at the genetic, cellular and developmental levels and we’ll undoubtedly learn much more about Wolbachia-host interactions. It’s pretty clear, though, that in general we can expect the effects of a novel Wolbachia infection to be associated with host as well as Wolbachia genotype.

    Male-killing is only one possible effect of Wolbachia. In some arthropods, it feminizes genetic males; in some others, it permits infected females to reproduce by parthenogenesis, and in still others, it causes matings between infected males and uninfected females to be reproductively unsuccessful. Other strains of Wolbachia infect filarial nematodes, and have become reproductive mutualists, but that’s another story. The important point is that Wolbachia‘s main function is to make more Wolbachia, and since its most efficient means of transmission is from mother to offspring, Wolbachia-host associations tend to evolve in a manner that favors infected female hosts.

  46. PMembrane says

    Without men, most engineers, chemists, physicists, computer scientists, surgeons, construction workers, maintenance workers, pilots, ship’s captains and crew, rail workers, architects, farmers, truckers, etc. etc. would be gone in short order.

    Women were able to take up many largely male occupations en masse in the United States in very short order when it joined WWII. Further, given that the story’s timeframe is 2002 and not 1952, there would be substantial numbers of women in all of the skilled professions listed above.

    It would be a very primitive life with little likelihood of improving, or finding a cure.

    Provided the huge political, psychological, and economic disruption did not cause public order to break down right at the outset, I don’t see why.

  47. raven says

    Without men, most engineers, chemists, physicists, computer scientists, surgeons, construction workers, maintenance workers, pilots, ship’s captains and crew, rail workers, architects, farmers, truckers, etc. etc. would be gone in short order.

    It would be a very primitive life with little likelihood of improving, or finding a cure.
    Hey! Would you empty that chamberpot, and patch up that thatched roof while you’re at it!
    Posted by: Rene

    The percentage of women graduating
    from U.S. medical schools rose from
    7.7% in 1964 to 45.1% in 2003.

    What century in the past are you posting from? Or are you from some dark ages place like Afghanistan or Kansas?

    Things have changed since then. In most professions such as medicine, law, etc.. the male to female ratio of new graduates approaches 50:50. And how hard is it to drive a truck anyway? Not very.

  48. says

    Has anyone mentioned this yet?

    http://www.abc.net.au/science/news/stories/s1710838.htm

    According to this professor, if Y is on its way to being phased out, perhaps other genes will take over “male” functions.

    #55: I’ve heard that argument a lot, too. However, I wonder if part of the reasons more women don’t enter the fields of math, engineering, etc. are: 1. the social negative-stereotype reinforcement factor (e.g. people don’t have as much faith in themselves if they keep hearing negative stereotypes about what their age, race, gender, etc. are supposedly aren’t capable of doing as well) and 2. not as much of a social reward incentive. Society tends to reward women more for social and superficial attributes whereas certain fields such as math and engineering require hours of solitary focus, (which has been more socially acceptable for a man, who is more traditionally seen in a “breadwinner” role.)

  49. says

    As Julie Stahlut mentions, Wolbachia was recently discovered to be a mutualist symbiont in filarial worms such as the guinea worm (a two-foot-long parasite of humans that lives under your skin and vomits out babies when you go for a swim to try and stop the intolerable itchiness of having a two-foot-long worm vomiting out babies under your skin)

    the remarkable thing they discovered is that taking a course of antibiotics can make these worms far, far less unpleasant. Indeed, Wolbachia has somehow made itself vital to the worm’s virulence!

    is very cool, in my opinion. Wolbachia and guinea worms FTW!

  50. Anonymous says

    Please dear god somebody make this a reality. Men are always going to be sexist assholes and I’m freaking sick to death of them.

  51. spondee says

    Somebody hasn’t been reading the later books…

    And honestly, the fact that Yorick’s father was among those killed, and that the only other survivor was Yoricks pet monkey points more towards acquired immunity over genetic mutation.

    However, since we know that when the plague hit it wiped out all males in gestation, he could father a bunch of daughters, with the male fetuses spontaneously aborting.

    But that would be a true give-away of his whereabouts. Leaving a trail of pregnant women in his wake would be like drawing a map for the bad-guys to follow.

  52. says

    Ken wrote re: Harlan Ellison’s movie ‘A Boy and His Dog’ “In the movie he ate the dog…” My recollection is that the girl said choose me or your dog, and the last scene was the boy and his dog munching on some very large drumsticks… (Ha! – I’m right – see http://en.wikipedia.org/wiki/A_Boy_and_His_Dog)

    Meanwhile, back to single-gender dystopias: I was also recalling how Rosie the Riveter and her sisters kept American industry going during WWII…I think women could do very well (again), thank you.

  53. Pierre says

    “I think women could do very well (again), thank you.”

    … but think of all the unopened pickle jars!

  54. Ack says

    And how hard is it to drive a truck anyway? Not very.
    perhaps you haven’t seen the new history channel effort:
    Ice Road Truckers!
    http://www.history.com/minisite.do?content_type=mini_home&mini_id=54692
    *sigh*
    the things the history channel wastes its money on these days.

    What, you’d rather it be on yet another poorly done documentary that partially glorifies Nazi Germany, or some pseudo-intellectual examination of the bible? Personally I think they should stick to the Ice Truckers.

  55. Syona says

    Actually, there is a way that the plague in Y could work… it’s not biological.

    What if the plague was in fact a self-replicating nanomachine, designed to do one simple task; infect everything it comes into contact with that has testosterone in it’s system, then latch onto the walls of blood vessels… and wait for a signal.

    When it receives a coded radio signal, the nanomachine self-destructs, blowing a hole in the wall of the blood vessel.

    Result, near instantaneously bleeding corpse of everything mammalian/avian and male. That is, if you can blanket the entire globe in one go with the trigger signal. Which would take a minimum of 4 geosynchronous communications satellites transmitting a piggybacked signal.

    Not that I’m saying that’s how it was done in the book… just playing ‘what if’ games here.